Allostatic-Interoceptive Overload in Frontotemporal Dementia
The predictive coding theory of allostatic-interoceptive load states that brain networks mediating autonomic regulation and interoceptive-exteroceptive balance regulate the internal milieu to anticipate future needs and environmental demands. These functions seem to be distinctly compromised in beha...
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| Veröffentlicht in: | Biological psychiatry (1969) 2022-07, Vol.92 (1), p.54-67 |
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| creator | Birba, Agustina Santamaría-García, Hernando Prado, Pavel Cruzat, Josefina Ballesteros, Agustín Sainz Legaz, Agustina Fittipaldi, Sol Duran-Aniotz, Claudia Slachevsky, Andrea Santibañez, Rodrigo Sigman, Mariano García, Adolfo M. Whelan, Robert Moguilner, Sebastián Ibáñez, Agustín |
| description | The predictive coding theory of allostatic-interoceptive load states that brain networks mediating autonomic regulation and interoceptive-exteroceptive balance regulate the internal milieu to anticipate future needs and environmental demands. These functions seem to be distinctly compromised in behavioral variant frontotemporal dementia (bvFTD), including alterations of the allostatic-interoceptive network (AIN). Here, we hypothesize that bvFTD is typified by an allostatic-interoceptive overload.
We assessed resting-state heartbeat evoked potential (rsHEP) modulation as well as its behavioral and multimodal neuroimaging correlates in patients with bvFTD relative to healthy control subjects and patients with Alzheimer’s disease (N = 94). We measured 1) resting-state electroencephalography (to assess the rsHEP, prompted by visceral inputs and modulated by internal body sensing), 2) associations between rsHEP and its neural generators (source location), 3) cognitive disturbances (cognitive state, executive functions, facial emotion recognition), 4) brain atrophy, and 5) resting-state functional magnetic resonance imaging functional connectivity (AIN vs. control networks).
Relative to healthy control subjects and patients with Alzheimer’s disease, patients with bvFTD presented more negative rsHEP amplitudes with sources in critical hubs of the AIN (insula, amygdala, somatosensory cortex, hippocampus, anterior cingulate cortex). This exacerbated rsHEP modulation selectively predicted the patients’ cognitive profile (including cognitive decline, executive dysfunction, and emotional impairments). In addition, increased rsHEP modulation in bvFTD was associated with decreased brain volume and connectivity of the AIN. Machine learning results confirmed AIN specificity in predicting the bvFTD group.
Altogether, these results suggest that bvFTD may be characterized by an allostatic-interoceptive overload manifested in ongoing electrophysiological markers, brain atrophy, functional networks, and cognition. |
| doi_str_mv | 10.1016/j.biopsych.2022.02.955 |
| format | Article |
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We assessed resting-state heartbeat evoked potential (rsHEP) modulation as well as its behavioral and multimodal neuroimaging correlates in patients with bvFTD relative to healthy control subjects and patients with Alzheimer’s disease (N = 94). We measured 1) resting-state electroencephalography (to assess the rsHEP, prompted by visceral inputs and modulated by internal body sensing), 2) associations between rsHEP and its neural generators (source location), 3) cognitive disturbances (cognitive state, executive functions, facial emotion recognition), 4) brain atrophy, and 5) resting-state functional magnetic resonance imaging functional connectivity (AIN vs. control networks).
Relative to healthy control subjects and patients with Alzheimer’s disease, patients with bvFTD presented more negative rsHEP amplitudes with sources in critical hubs of the AIN (insula, amygdala, somatosensory cortex, hippocampus, anterior cingulate cortex). This exacerbated rsHEP modulation selectively predicted the patients’ cognitive profile (including cognitive decline, executive dysfunction, and emotional impairments). In addition, increased rsHEP modulation in bvFTD was associated with decreased brain volume and connectivity of the AIN. Machine learning results confirmed AIN specificity in predicting the bvFTD group.
Altogether, these results suggest that bvFTD may be characterized by an allostatic-interoceptive overload manifested in ongoing electrophysiological markers, brain atrophy, functional networks, and cognition.</description><identifier>ISSN: 0006-3223</identifier><identifier>ISSN: 1873-2402</identifier><identifier>EISSN: 1873-2402</identifier><identifier>DOI: 10.1016/j.biopsych.2022.02.955</identifier><identifier>PMID: 35491275</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Allostasis ; Allostatic-interoceptive network ; Alzheimer Disease - pathology ; Atrophy - pathology ; Brain ; Brain Mapping ; Frontotemporal dementia ; Frontotemporal Dementia - diagnostic imaging ; Frontotemporal Dementia - pathology ; HEP ; Humans ; Interoception ; Magnetic Resonance Imaging ; Multimodal imaging ; Predictive coding ; rsHEP</subject><ispartof>Biological psychiatry (1969), 2022-07, Vol.92 (1), p.54-67</ispartof><rights>2022 Society of Biological Psychiatry</rights><rights>Copyright © 2022 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c472t-ca8c7b27c406d811818a3df06bc0fb546e707a0c2373b35c5d77ed7f751513ce3</citedby><cites>FETCH-LOGICAL-c472t-ca8c7b27c406d811818a3df06bc0fb546e707a0c2373b35c5d77ed7f751513ce3</cites><orcidid>0000-0003-1314-0435 ; 0000-0001-6758-5101 ; 0000-0002-1324-6400 ; 0000-0003-2503-8366 ; 0000-0002-6936-0114 ; 0000-0002-2391-4468</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0006322322010423$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35491275$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Birba, Agustina</creatorcontrib><creatorcontrib>Santamaría-García, Hernando</creatorcontrib><creatorcontrib>Prado, Pavel</creatorcontrib><creatorcontrib>Cruzat, Josefina</creatorcontrib><creatorcontrib>Ballesteros, Agustín Sainz</creatorcontrib><creatorcontrib>Legaz, Agustina</creatorcontrib><creatorcontrib>Fittipaldi, Sol</creatorcontrib><creatorcontrib>Duran-Aniotz, Claudia</creatorcontrib><creatorcontrib>Slachevsky, Andrea</creatorcontrib><creatorcontrib>Santibañez, Rodrigo</creatorcontrib><creatorcontrib>Sigman, Mariano</creatorcontrib><creatorcontrib>García, Adolfo M.</creatorcontrib><creatorcontrib>Whelan, Robert</creatorcontrib><creatorcontrib>Moguilner, Sebastián</creatorcontrib><creatorcontrib>Ibáñez, Agustín</creatorcontrib><title>Allostatic-Interoceptive Overload in Frontotemporal Dementia</title><title>Biological psychiatry (1969)</title><addtitle>Biol Psychiatry</addtitle><description>The predictive coding theory of allostatic-interoceptive load states that brain networks mediating autonomic regulation and interoceptive-exteroceptive balance regulate the internal milieu to anticipate future needs and environmental demands. These functions seem to be distinctly compromised in behavioral variant frontotemporal dementia (bvFTD), including alterations of the allostatic-interoceptive network (AIN). Here, we hypothesize that bvFTD is typified by an allostatic-interoceptive overload.
We assessed resting-state heartbeat evoked potential (rsHEP) modulation as well as its behavioral and multimodal neuroimaging correlates in patients with bvFTD relative to healthy control subjects and patients with Alzheimer’s disease (N = 94). We measured 1) resting-state electroencephalography (to assess the rsHEP, prompted by visceral inputs and modulated by internal body sensing), 2) associations between rsHEP and its neural generators (source location), 3) cognitive disturbances (cognitive state, executive functions, facial emotion recognition), 4) brain atrophy, and 5) resting-state functional magnetic resonance imaging functional connectivity (AIN vs. control networks).
Relative to healthy control subjects and patients with Alzheimer’s disease, patients with bvFTD presented more negative rsHEP amplitudes with sources in critical hubs of the AIN (insula, amygdala, somatosensory cortex, hippocampus, anterior cingulate cortex). This exacerbated rsHEP modulation selectively predicted the patients’ cognitive profile (including cognitive decline, executive dysfunction, and emotional impairments). In addition, increased rsHEP modulation in bvFTD was associated with decreased brain volume and connectivity of the AIN. Machine learning results confirmed AIN specificity in predicting the bvFTD group.
Altogether, these results suggest that bvFTD may be characterized by an allostatic-interoceptive overload manifested in ongoing electrophysiological markers, brain atrophy, functional networks, and cognition.</description><subject>Allostasis</subject><subject>Allostatic-interoceptive network</subject><subject>Alzheimer Disease - pathology</subject><subject>Atrophy - pathology</subject><subject>Brain</subject><subject>Brain Mapping</subject><subject>Frontotemporal dementia</subject><subject>Frontotemporal Dementia - diagnostic imaging</subject><subject>Frontotemporal Dementia - pathology</subject><subject>HEP</subject><subject>Humans</subject><subject>Interoception</subject><subject>Magnetic Resonance Imaging</subject><subject>Multimodal imaging</subject><subject>Predictive coding</subject><subject>rsHEP</subject><issn>0006-3223</issn><issn>1873-2402</issn><issn>1873-2402</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkE1LxDAQhoMoun78Bdmjl9Z8NE0FQUVdFQQveg7pdOpmaZuaZBf892bZVfTkaRjmnfedeQg5ZTRnlJXni7y2bgyfMM855TynPL-QcodMWKVExgvKd8mEUlpmgnNxQA5DWKRWcc72yYGQxQXjSk7I5U3XuRBNtJA9DRG9AxyjXeH0ZYW-c6aZ2mE6826ILmI_Om-66R32OERrjslea7qAJ9t6RN5m96-3j9nzy8PT7c1zBoXiMQNTgaq5goKWTcVYxSojmpaWNdC2lkWJiipDgQslaiFBNkpho1olmWQCUByRq43vuKx7bCCFpzP06G1v_Kd2xuq_k8HO9btbaZbC0qdVcjjbOnj3scQQdW8DYNeZAd0yaF7KqiwKJmmSlhspeBeCx_Ynh1G9Zq8X-pu9XrPXlOvEPi2e_r7yZ-0bdhJcbwSYWK0seh3A4gDYWI8QdePsfxlfWa6afQ</recordid><startdate>20220701</startdate><enddate>20220701</enddate><creator>Birba, Agustina</creator><creator>Santamaría-García, Hernando</creator><creator>Prado, Pavel</creator><creator>Cruzat, Josefina</creator><creator>Ballesteros, Agustín Sainz</creator><creator>Legaz, Agustina</creator><creator>Fittipaldi, Sol</creator><creator>Duran-Aniotz, Claudia</creator><creator>Slachevsky, Andrea</creator><creator>Santibañez, Rodrigo</creator><creator>Sigman, Mariano</creator><creator>García, Adolfo M.</creator><creator>Whelan, Robert</creator><creator>Moguilner, Sebastián</creator><creator>Ibáñez, Agustín</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-1314-0435</orcidid><orcidid>https://orcid.org/0000-0001-6758-5101</orcidid><orcidid>https://orcid.org/0000-0002-1324-6400</orcidid><orcidid>https://orcid.org/0000-0003-2503-8366</orcidid><orcidid>https://orcid.org/0000-0002-6936-0114</orcidid><orcidid>https://orcid.org/0000-0002-2391-4468</orcidid></search><sort><creationdate>20220701</creationdate><title>Allostatic-Interoceptive Overload in Frontotemporal Dementia</title><author>Birba, Agustina ; 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These functions seem to be distinctly compromised in behavioral variant frontotemporal dementia (bvFTD), including alterations of the allostatic-interoceptive network (AIN). Here, we hypothesize that bvFTD is typified by an allostatic-interoceptive overload.
We assessed resting-state heartbeat evoked potential (rsHEP) modulation as well as its behavioral and multimodal neuroimaging correlates in patients with bvFTD relative to healthy control subjects and patients with Alzheimer’s disease (N = 94). We measured 1) resting-state electroencephalography (to assess the rsHEP, prompted by visceral inputs and modulated by internal body sensing), 2) associations between rsHEP and its neural generators (source location), 3) cognitive disturbances (cognitive state, executive functions, facial emotion recognition), 4) brain atrophy, and 5) resting-state functional magnetic resonance imaging functional connectivity (AIN vs. control networks).
Relative to healthy control subjects and patients with Alzheimer’s disease, patients with bvFTD presented more negative rsHEP amplitudes with sources in critical hubs of the AIN (insula, amygdala, somatosensory cortex, hippocampus, anterior cingulate cortex). This exacerbated rsHEP modulation selectively predicted the patients’ cognitive profile (including cognitive decline, executive dysfunction, and emotional impairments). In addition, increased rsHEP modulation in bvFTD was associated with decreased brain volume and connectivity of the AIN. Machine learning results confirmed AIN specificity in predicting the bvFTD group.
Altogether, these results suggest that bvFTD may be characterized by an allostatic-interoceptive overload manifested in ongoing electrophysiological markers, brain atrophy, functional networks, and cognition.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>35491275</pmid><doi>10.1016/j.biopsych.2022.02.955</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0003-1314-0435</orcidid><orcidid>https://orcid.org/0000-0001-6758-5101</orcidid><orcidid>https://orcid.org/0000-0002-1324-6400</orcidid><orcidid>https://orcid.org/0000-0003-2503-8366</orcidid><orcidid>https://orcid.org/0000-0002-6936-0114</orcidid><orcidid>https://orcid.org/0000-0002-2391-4468</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Allostasis Allostatic-interoceptive network Alzheimer Disease - pathology Atrophy - pathology Brain Brain Mapping Frontotemporal dementia Frontotemporal Dementia - diagnostic imaging Frontotemporal Dementia - pathology HEP Humans Interoception Magnetic Resonance Imaging Multimodal imaging Predictive coding rsHEP |
| title | Allostatic-Interoceptive Overload in Frontotemporal Dementia |
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